Phân nhóm và phân chức năng của họ protein RIFIN nhiều bản sao

Springer Science and Business Media LLC - Tập 9 Số 1 - 2008
Nicolas Joannin1, Saraswathi Abhiman2, Erik L. L. Sonnhammer2, Mats Wahlgren1
1Department of Microbiology, Tumor and Cell biology (MTC), Karolinska Institutet, Sweden and Swedish Institute for Infectious Diseases Control, SE-17177 Stockholm, SE-17182, Stockholm, Sweden
2Stockholm Bioinformatics Center, AlbaNova University Center, Stockholm University, SE-106 91, Stockholm, Sweden

Tóm tắt

Tóm tắt Đặt vấn đề Các nguyên sinh động vật ký sinh sở hữu nhiều họ gen sao chép dẫn xuất mà có vai trò trung tâm trong sự sống sót và độc lực của ký sinh trùng. Số lượng và sự biến đổi của các thành viên trong những họ gen này thường khiến việc dự đoán chức năng có thể của các protein được mã hóa trở nên khó khăn. Các họ protein ngoại bào tiếp xúc với phản ứng miễn dịch của vật chủ đã được chọn lọc qua cơ chế miễn dịch để trở nên biến thể kháng nguyên, từ đó tránh được sự nhận diện miễn dịch trong khi vẫn duy trì chức năng protein nhằm thiết lập một nhiễm trùng mạn tính. Kết quả Chúng tôi đã kết hợp phân tích tiến hóa và phân tích chuyển chức năng để nghiên cứu sự tiến hóa của các protein RIFIN, là những loại protein biến thể kháng nguyên và được mã hóa bởi họ gen sao chép lớn nhất trong Plasmodium falciparum. Chúng tôi cho thấy rằng họ này có thể được phân chia thành hai nhóm chính mà chúng tôi đã đặt tên là protein A- và B-RIFIN. Sự phân nhóm được đề xuất này được hỗ trợ bởi một nghiên cứu gần đây đã chỉ ra rằng, mặc dù có sự hiện diện của động cơ xuất khẩu Plasmodium (PEXEL) ở tất cả các biến thể RIFIN, nhưng các protein từ mỗi nhóm có các vị trí phân bố tế bào khác nhau trong chu kỳ sống trong hồng cầu của ký sinh trùng. Trong nghiên cứu hiện tại, chúng tôi cho thấy rằng phân tích chuyển chức năng, một kỹ thuật mới dự đoán sự khác biệt chức năng giữa các nhóm phụ của một họ protein, chỉ ra rằng các RIFIN đã trải qua sự neo hoặc phụ chức năng.

Từ khóa

#RIFIN #protein multi-copy #phân tích phylogenetic #chức năng protein #Plasmodium falciparum

Tài liệu tham khảo

Stringer JR, Keely SP: Genetics of surface antigen expression in Pneumocystis carinii. Infect Immun. 2001, 69 (2): 627-639. 10.1128/IAI.69.2.627-639.2001.

Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL, Craig A, Kyes S, Chan MS, Nene V, Shallom SJ, Suh B, Peterson J, Angiuoli S, Pertea M, Allen J, Selengut J, Haft D, Mather MW, Vaidya AB, Martin DM, Fairlamb AH, Fraunholz MJ, Roos DS, Ralph SA, McFadden GI, Cummings LM, Subramanian GM, Mungall C, Venter JC, Carucci DJ, Hoffman SL, Newbold C, Davis RW, Fraser CM, Barrell B: Genome sequence of the human malaria parasite Plasmodium falciparum. Nature. 2002, 419 (6906): 498-511. 10.1038/nature01097.

del Portillo HA, Fernandez-Becerra C, Bowman S, Oliver K, Preuss M, Sanchez CP, Schneider NK, Villalobos JM, Rajandream MA, Harris D, Pereira da Silva LH, Barrell B, Lanzer M: A superfamily of variant genes encoded in the subtelomeric region of Plasmodium vivax. Nature. 2001, 410 (6830): 839-842. 10.1038/35071118.

Fischer K, Chavchich M, Huestis R, Wilson DW, Kemp DJ, Saul A: Ten families of variant genes encoded in subtelomeric regions of multiple chromosomes of Plasmodium chabaudi, a malaria species that undergoes antigenic variation in the laboratory mouse. Mol Microbiol. 2003, 48 (5): 1209-1223. 10.1046/j.1365-2958.2003.03491.x.

Janssen CS, Phillips RS, Turner CM, Barrett MP: Plasmodium interspersed repeats: the major multigene superfamily of malaria parasites. Nucleic Acids Res. 2004, 32 (19): 5712-5720. 10.1093/nar/gkh907.

Sam-Yellowe TY, Florens L, Johnson JR, Wang T, Drazba JA, Le Roch KG, Zhou Y, Batalov S, Carucci DJ, Winzeler EA, Yates JR: A Plasmodium gene family encoding Maurer's cleft membrane proteins: structural properties and expression profiling. Genome Res. 2004, 14 (6): 1052-1059. 10.1101/gr.2126104.

Chen Q, Fernandez V, Sundstrom A, Schlichtherle M, Datta S, Hagblom P, Wahlgren M: Developmental selection of var gene expression in Plasmodium falciparum. Nature. 1998, 394 (6691): 392-395. 10.1038/28660.

Fernandez V, Hommel M, Chen Q, Hagblom P, Wahlgren M: Small, clonally variant antigens expressed on the surface of the Plasmodium falciparum-infected erythrocyte are encoded by the rif gene family and are the target of human immune responses. J Exp Med. 1999, 190 (10): 1393-1404. 10.1084/jem.190.10.1393.

Kyes SA, Rowe JA, Kriek N, Newbold CI: Rifins: a second family of clonally variant proteins expressed on the surface of red cells infected with Plasmodium falciparum. Proc Natl Acad Sci U S A. 1999, 96 (16): 9333-9338. 10.1073/pnas.96.16.9333.

Scherf A, Hernandez-Rivas R, Buffet P, Bottius E, Benatar C, Pouvelle B, Gysin J, Lanzer M: Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum. Embo J. 1998, 17 (18): 5418-5426. 10.1093/emboj/17.18.5418.

Freitas-Junior LH, Bottius E, Pirrit LA, Deitsch KW, Scheidig C, Guinet F, Nehrbass U, Wellems TE, Scherf A: Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum. Nature. 2000, 407 (6807): 1018-1022. 10.1038/35039531.

Hernandez-Rivas R, Hinterberg K, Scherf A: Compartmentalization of genes coding for immunodominant antigens to fragile chromosome ends leads to dispersed subtelomeric gene families and rapid gene evolution in Plasmodium falciparum. Mol Biochem Parasitol. 1996, 78 (1-2): 137-148. 10.1016/S0166-6851(96)02618-7.

Rasti N, Wahlgren M, Chen Q: Molecular aspects of malaria pathogenesis. FEMS Immunol Med Microbiol. 2004, 41 (1): 9-26. 10.1016/j.femsim.2004.01.010.

Robinson BA, Welch TL, Smith JD: Widespread functional specialization of Plasmodium falciparum erythrocyte membrane protein 1 family members to bind CD36 analysed across a parasite genome. Mol Microbiol. 2003, 47 (5): 1265-1278. 10.1046/j.1365-2958.2003.03378.x.

Cheng Q, Cloonan N, Fischer K, Thompson J, Waine G, Lanzer M, Saul A: stevor and rif are Plasmodium falciparum multicopy gene families which potentially encode variant antigens. Mol Biochem Parasitol. 1998, 97 (1-2): 161-176. 10.1016/S0166-6851(98)00144-3.

Gardner MJ, Tettelin H, Carucci DJ, Cummings LM, Aravind L, Koonin EV, Shallom S, Mason T, Yu K, Fujii C, Pederson J, Shen K, Jing J, Aston C, Lai Z, Schwartz DC, Pertea M, Salzberg S, Zhou L, Sutton GG, Clayton R, White O, Smith HO, Fraser CM, Adams MD, Venter JC, Hoffman SL: Chromosome 2 sequence of the human malaria parasite Plasmodium falciparum. Science. 1998, 282 (5391): 1126-1132. 10.1126/science.282.5391.1126.

Finn RD, Mistry J, Schuster-Bockler B, Griffiths-Jones S, Hollich V, Lassmann T, Moxon S, Marshall M, Khanna A, Durbin R, Eddy SR, Sonnhammer EL, Bateman A: Pfam: clans, web tools and services. Nucleic Acids Res. 2006, 34 (Database issue): D247-51. 10.1093/nar/gkj149.

Florens L, Washburn MP, Raine JD, Anthony RM, Grainger M, Haynes JD, Moch JK, Muster N, Sacci JB, Tabb DL, Witney AA, Wolters D, Wu Y, Gardner MJ, Holder AA, Sinden RE, Yates JR, Carucci DJ: A proteomic view of the Plasmodium falciparum life cycle. Nature. 2002, 419 (6906): 520-526. 10.1038/nature01107.

Haeggstrom M, Kironde F, Berzins K, Chen Q, Wahlgren M, Fernandez V: Common trafficking pathway for variant antigens destined for the surface of the Plasmodium falciparum-infected erythrocyte. Mol Biochem Parasitol. 2004, 133 (1): 1-14. 10.1016/j.molbiopara.2003.07.006.

Helmby H, Cavelier L, Pettersson U, Wahlgren M: Rosetting Plasmodium falciparum-infected erythrocytes express unique strain-specific antigens on their surface. Infect Immun. 1993, 61 (1): 284-288.

Petter M, Haeggstrom M, Khattab A, Fernandez V, Klinkert MQ, Wahlgren M: Variant proteins of the Plasmodium falciparum RIFIN family show distinct subcellular localization and developmental expression patterns. Mol Biochem Parasitol. 2007, 156 (1): 51-61. 10.1016/j.molbiopara.2007.07.011.

Abdel-Latif MS, Dietz K, Issifou S, Kremsner PG, Klinkert MQ: Antibodies to Plasmodium falciparum rifin proteins are associated with rapid parasite clearance and asymptomatic infections. Infect Immun. 2003, 71 (11): 6229-6233. 10.1128/IAI.71.11.6229-6233.2003.

Abdel-Latif MS, Khattab A, Lindenthal C, Kremsner PG, Klinkert MQ: Recognition of variant Rifin antigens by human antibodies induced during natural Plasmodium falciparum infections. Infect Immun. 2002, 70 (12): 7013-7021. 10.1128/IAI.70.12.7013-7021.2002.

Marti M, Good RT, Rug M, Knuepfer E, Cowman AF: Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science. 2004, 306 (5703): 1930-1933. 10.1126/science.1102452.

Tham WH, Payne PD, Brown GV, Rogerson SJ: Identification of basic transcriptional elements required for rif gene transcription. Int J Parasitol. 2007, 37 (6): 605-615. 10.1016/j.ijpara.2006.11.006.

Abhiman S, Sonnhammer EL: Large-scale prediction of function shift in protein families with a focus on enzymatic function. Proteins. 2005, 60 (4): 758-768. 10.1002/prot.20550.

Knudsen B, Miyamoto MM: A likelihood ratio test for evolutionary rate shifts and functional divergence among proteins. Proc Natl Acad Sci U S A. 2001, 98 (25): 14512-14517. 10.1073/pnas.251526398.

Prim N, Bofill C, Pastor FI, Diaz P: Esterase EstA6 from Pseudomonas sp. CR-611 is a novel member in the utmost conserved cluster of family VI bacterial lipolytic enzymes. Biochimie. 2006, 88 (7): 859-867. 10.1016/j.biochi.2006.02.011.

Stam MR, Danchin EG, Rancurel C, Coutinho PM, Henrissat B: Dividing the large glycoside hydrolase family 13 into subfamilies: towards improved functional annotations of alpha-amylase-related proteins. Protein Eng Des Sel. 2006, 19 (12): 555-562. 10.1093/protein/gzl044.

Khattab A, Klinkert MQ: Maurer's clefts-restricted localization, orientation and export of a Plasmodium falciparum RIFIN. Traffic. 2006, 7 (12): 1654-1665. 10.1111/j.1600-0854.2006.00494.x.

Kraemer SM, Smith JD: Evidence for the importance of genetic structuring to the structural and functional specialization of the Plasmodium falciparum var gene family. Mol Microbiol. 2003, 50 (5): 1527-1538. 10.1046/j.1365-2958.2003.03814.x.

DePristo MA, Zilversmit MM, Hartl DL: On the abundance, amino acid composition, and evolutionary dynamics of low-complexity regions in proteins. Gene. 2006, 378: 19-30. 10.1016/j.gene.2006.03.023.

Enea V, Corredor V: The evolution of plasmodial stage-specific rRNA genes is dominated by gene conversion. J Mol Evol. 1991, 32 (2): 183-186. 10.1007/BF02515391.

Nielsen KM, Kasper J, Choi M, Bedford T, Kristiansen K, Wirth DF, Volkman SK, Lozovsky ER, Hartl DL: Gene conversion as a source of nucleotide diversity in Plasmodium falciparum. Mol Biol Evol. 2003, 20 (5): 726-734. 10.1093/molbev/msg076.

Posada D, Crandall KA: The effect of recombination on the accuracy of phylogeny estimation. J Mol Evol. 2002, 54 (3): 396-402.

Kennedy M, Holland BR, Gray RD, Spencer HG: Untangling long branches: identifying conflicting phylogenetic signals using spectral analysis, neighbor-net, and consensus networks. Syst Biol. 2005, 54 (4): 620-633. 10.1080/106351591007462.

Stiller JW, Hall BD: Long-branch attraction and the rDNA model of early eukaryotic evolution. Mol Biol Evol. 1999, 16 (9): 1270-1279.

Shakhnovich BE, Koonin EV: Origins and impact of constraints in evolution of gene families. Genome Res. 2006, 16 (12): 1529-1536. 10.1101/gr.5346206.

Lavstsen T, Salanti A, Jensen AT, Arnot DE, Theander TG: Sub-grouping of Plasmodium falciparum 3D7 var genes based on sequence analysis of coding and non-coding regions. Malar J. 2003, 2: 27-10.1186/1475-2875-2-27.

Voss TS, Thompson JK, Waterkeyn J, Felger I, Weiss N, Cowman AF, Beck HP: Genomic distribution and functional characterisation of two distinct and conserved Plasmodium falciparum var gene 5' flanking sequences. Mol Biochem Parasitol. 2000, 107 (1): 103-115. 10.1016/S0166-6851(00)00176-6.

Fonager J, Cunningham D, Jarra W, Koernig S, Henneman AA, Langhorne J, Preiser P: Transcription and alternative splicing in the yir multigene family of the malaria parasite Plasmodium y. yoelii: identification of motifs suggesting epigenetic and post-transcriptional control of RNA expression. Mol Biochem Parasitol. 2007, 156 (1): 1-11. 10.1016/j.molbiopara.2007.06.006.

Hiller NL, Bhattacharjee S, van Ooij C, Liolios K, Harrison T, Lopez-Estrano C, Haldar K: A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science. 2004, 306 (5703): 1934-1937. 10.1126/science.1102737.

Golding GB, Dean AM: The structural basis of molecular adaptation. Mol Biol Evol. 1998, 15 (4): 355-369.

DePristo MA, Weinreich DM, Hartl DL: Missense meanderings in sequence space: a biophysical view of protein evolution. Nat Rev Genet. 2005, 6 (9): 678-687. 10.1038/nrg1672.

Weber JL: Interspersed repetitive DNA from Plasmodium falciparum. Mol Biochem Parasitol. 1988, 29 (2-3): 117-124. 10.1016/0166-6851(88)90066-7.

Bozdech Z, Llinas M, Pulliam BL, Wong ED, Zhu J, DeRisi JL: The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol. 2003, 1 (1): E5-10.1371/journal.pbio.0000005.

Daily JP, Le Roch KG, Sarr O, Ndiaye D, Lukens A, Zhou Y, Ndir O, Mboup S, Sultan A, Winzeler EA, Wirth DF: In vivo transcriptome of Plasmodium falciparum reveals overexpression of transcripts that encode surface proteins. J Infect Dis. 2005, 191 (7): 1196-1203. 10.1086/428289.

Le Roch KG, Zhou Y, Blair PL, Grainger M, Moch JK, Haynes JD, De La Vega P, Holder AA, Batalov S, Carucci DJ, Winzeler EA: Discovery of gene function by expression profiling of the malaria parasite life cycle. Science. 2003, 301 (5639): 1503-1508. 10.1126/science.1087025.

Llinas M, Bozdech Z, Wong ED, Adai AT, DeRisi JL: Comparative whole genome transcriptome analysis of three Plasmodium falciparum strains. Nucleic Acids Res. 2006, 34 (4): 1166-1173. 10.1093/nar/gkj517.

Fernandez-Becerra C, Pein O, de Oliveira TR, Yamamoto MM, Cassola AC, Rocha C, Soares IS, de Braganca Pereira CA, del Portillo HA: Variant proteins of Plasmodium vivax are not clonally expressed in natural infections. Mol Microbiol. 2005, 58 (3): 648-658. 10.1111/j.1365-2958.2005.04850.x.

Preiser PR, Khan S, Costa FT, Jarra W, Belnoue E, Ogun S, Holder AA, Voza T, Landau I, Snounou G, Renia L: Stage-specific transcription of distinct repertoires of a multigene family during Plasmodium life cycle. Science. 2002, 295 (5553): 342-345. 10.1126/science.1064938.

PlasmoDB v4.4. [http://v4-4.plasmodb.org/]

Broad Institute of Harvard and M.I.T. [http://www.broad.mit.edu/]

Lassmann T, Sonnhammer EL: Kalign--an accurate and fast multiple sequence alignment algorithm. BMC Bioinformatics. 2005, 6: 298-10.1186/1471-2105-6-298.

Hall T: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser. 1999, 41: 95-98.

GeneDB. [http://www.genedb.org/]

Suyama M, Torrents D, Bork P: PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 2006, 34 (Web Server issue): W609-12. 10.1093/nar/gkl315.

Kumar S, Tamura K, Nei M: MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform. 2004, 5 (2): 150-163. 10.1093/bib/5.2.150.

Protein Sequence Logos and Relative Entropy. [http://www.cbs.dtu.dk/~gorodkin/appl/plogo.html]

Schneider TD, Stephens RM: Sequence logos: a new way to display consensus sequences. Nucleic Acids Res. 1990, 18 (20): 6097-6100. 10.1093/nar/18.20.6097.

Bryson K, McGuffin LJ, Marsden RL, Ward JJ, Sodhi JS, Jones DT: Protein structure prediction servers at University College London. Nucleic Acids Res. 2005, 33 (Web Server issue): W36-8. 10.1093/nar/gki410.

Jones DT: Protein secondary structure prediction based on position-specific scoring matrices. Journal of molecular biology. 1999, 292 (2): 195-202. 10.1006/jmbi.1999.3091.

Clamp M, Cuff J, Searle SM, Barton GJ: The Jalview Java alignment editor. Bioinformatics (Oxford, England). 2004, 20 (3): 426-427. 10.1093/bioinformatics/btg430.

Thông tin
Thông tin xuất bản

Springer Science and Business Media LLC

Tập 9 Số 1

Thông tin tác giả